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An Updated Investigation on the Dromedary Camel Cerebellum (Camelus Dromedarius) with Special Insight Into the Distribution of Calcium‑Binding Proteins Abdelraheim H

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An Updated Investigation on the Dromedary Camel Cerebellum (Camelus Dromedarius) with Special Insight Into the Distribution of Calcium‑Binding Proteins Abdelraheim H www.nature.com/scientificreports OPEN An updated investigation on the dromedary camel cerebellum (Camelus dromedarius) with special insight into the distribution of calcium‑binding proteins Abdelraheim H. Attaai1,3, Ahmed E. Noreldin2, Fatma M. Abdel‑maksoud1* & Manal T. Hussein1,3 Studying the cerebella of diferent animals is important to expand the knowledge about the cerebellum. Studying the camel cerebellum was neglected even though the recent research in the middle east and Asia. Therefore, the present study was designed to achieve a detailed description of the morphology and the cellular organization of the camel cerebellum. Because of the high importance of the calcium ions as a necessary moderator the current work also aimed to investigate the distribution of calcium binding proteins (CaBP) such as calbindin D‑28K (CB), parvalbumin (PV) and calretinin (CR) in diferent cerebellar cells including the non‑traditional neurons. The architecture of camel cerebellum, as diferent mammals, consists of the medulla and three layered‑cortex. According to our observation the cells in the granular layer were not crowded and many spaces were observed. CB expression was the highest by Purkinje cells including their dendritic arborization. In addition to its expression by the inhibitory interneurons (basket, stellate and Golgi neurons), it is also expressed by the excitatory granule cells. PV was expressed by Purkinje cells, including their primary arborization, and by the molecular layer cells. CR immunoreactivity (‑ir) was obvious in almost all cell layers with varying degrees, however a weak or any expression by the Purkinje cells. The molecular layer cells and the Golgi and the non traditional large neurons of the granular layer showed the strongest CR‑ir. Granule neurons showed moderate immunoreactivity for CB and CR. In conclusion, the results of the current study achieved a complete map for the neurochemical organization of CaBP expression and distribution by diferent cells in the camel cerebellum. Te cerebellum plays a fundamental role for diverse motor functions, postural control, balance, and motor coordination1,2. It is also involved in cognitive functions such as language, learning, memory, and some emo- tional behaviors such as fear3,4. Te cerebellum consists of 2 main components, the cerebellar cortex and the medulla. Tere are several cellular components in the cerebellar cortex; the most distinguished morphologically are Purkinje cells (PCs), granule, Golgi and basket cells 5. Tis complex neural network gives rise to a massive signal-processing capability that plays a role in motor learning 6. Te inputs to the cerebellum come from the climbing fbers and the mossy fbers. Most of the neuronal subtypes in the cerebellar cortex are interneurons which synapse with PCs. Te later’s axons constitute the outputs, of the integrated signals, which rely on either small deep cerebellar nuclei lying in the interior of the cerebellum or transmit information to structures outside the cerebellum. 1Department of Anatomy and Histology, Faculty of Veterinary Medicine, Assiut University, 71526 Assiut, Egypt. 2Department of Histology and Cytology, Faculty of Veterinary Medicine, Damanhour University, 22511 Damanhour, Egypt. 3These authors contributed equally: Manal T. Hussein and Abdelraheim H. Attaai. *email: [email protected] Scientifc Reports | (2020) 10:21157 | https://doi.org/10.1038/s41598-020-78192-7 1 Vol.:(0123456789) www.nature.com/scientificreports/ Calcium ions (Ca +2) are an important moderators, acting as major secondary messengers, of several vital physiological processes, including diferentiation and morphogenesis, membrane excitability and conductivity, axonal transport, synthesis and release of neuroactive substances and some neurotransmitters (phenomena of synaptic plasticity). Te calcium signal is mediated by a superfamily of structurally related proteins, generally known as calcium-binding proteins (CaBP), such as CB, PV, CR and S100 protein7–11. Tese molecules pos- sess characteristic structures which can bind Ca +2 with high afnity 12–14. Altered CaBP expression may lead to pathological and neurodegenerative conditions, such as in patients sufering from epileptic seizures are lacking neuronal PV15–17. It is important to study the cerebella of diferent animals, in order to expand our knowledge about the cerebellum and many cerebella of diferent species have been studied. However, there is a paucity of information concerning the morphology of camel cerebellum, even in the Middle East and Asia, where camels are important in their economies. It will be interesting to explore the cerebellum of an animal such as the drom- edary, with very long legs and neck, who lives in a hot desert and walks long distances under hard conditions. All these factors may require specialized architecture in its cerebellum. Terefore, the present study was designed to achieve a detailed description of the morphology and cellular organization of the camel cerebellum. Because of the high importance of the calcium ions as a necessary moderator the current work also aimed to investigate the distribution of calcium binding proteins (CaBP) such as calbindin D-28K (CB), parvalbumin (PV) and calretinin (CR) in diferent cerebellar cells including the non-traditional neurons. Material and methods Collection of specimens. Te Ethics Committee of Alexandria University, Egypt approved this study. In this study camel’s brain were collected from ten clinically healthy mature camels (Camelus dromedarius) (4–6 years old) heads without sex diferentiation. Te animals were sacrifced in Alexandria slaughterhouse in Alexandria province, Egypt according to local ethical board guidelines of Egyptian slaughterhouses (Alexandria animal ethics committee 24122018). Afer slaughtering the camel, the entire head was separated from the neck, and saline was injected in the common carotid artery to wash the blood from the head circulation. Te 4% para- formaldehyde in PBS was injected in the common carotid artery for at least 30 min then the skull was opened to obtain the brain. Every brain was hemisected into two halves before immersed in the same fxative to allow more exposure to the fxative. Afer have been stored at 4° C for 3 days. Te cerebellum was carefully dissected from the brain and the weight of the brain and the cerebellum were weighed using sensitive balance. Light microscopic study. Te tissue blocks were prepared for parafn cutting. Briefy, the dehydration of the fxed tissues was carried out using ascending grades of ethyl alcohol. Te samples were cleared by immers- ing in xylene then embedding in parafn wax (Sigma Aldrich, USA) according to the standard methodology described by Romeis18. Step serial sagittal Sects. (100 serial sections) from the vermal region of folia VI, VII, VIII were cut at 6–8 µm thickness using a Richert Leica RM 2125 Microtome, Germany, and mounted on glass slides. Some sections were stained with cresyl violet (to stain cell bodies) together with luxol fast blue (for myelinated fbers) and other section with Grimelius silver nitrate impregnation (for both cell bodies and processes)19. Immunohistochemical staining. Immunohistochemical staining had been performed on the parafn blocks as mentioned before by Abdel-Maksoud, et al.20. Sections were deparafnized with xylene and hydrated with a descending grade of ethanol then washed with 0.1 M PBS (3 × 10 min). To decrease the masking of anti- gen epitopes, the antigen retrieval was carried out using 0.1 M sodium citrate bufer solution (pH = 6) for 7 min using a microwave (600 W). Ten, sections were cooled to room temperature for 20 min and washed with PBS (pH 7.4) for 10 min. Afer blocking the endogenous peroxidase activity with 3% H 2O2 in H2O for 30 min at the room temperature (RT), the sections were washed with PBS (3 × 5 min), then the sections were blocked with 10% normal donkey serum (NDS) + 0.2% Triton-X100/PBS for 2 h at RT. Subsequently, sections were incubated overnight at 4 °C with the following antibodies: rabbit polyclonal anti-CB [1:200, Genemed Biotechnologies, cat- alogue NO. (61-0061)], rabbit polyclonal anti-PV [1:200, Termo Fisher Scientifc catalogue NO. (PA1-3945)] and mouse monoclonal anti-CR [1:200, Termo Fisher Scientifc; catalogue NO. (MA1-16629)]. Sections were rinsed 3 × 10 min in 0.2% Triton-X 100/PBS and incubated with biotinylated IgG goat anti-rabbit (catalogue NO.E043201-8) and IgG goat anti-mouse secondary antibody (catalogue NO.P0447) (from Dako, Hamburg, Germany) diluted at 1:200 for 2 h at RT, followed by incubation with Vectastain ABC (Avidin–Biotin complex) reagent for 45 min in a humid chamber at room temperature. Visualization of the reaction was carried out with 0.04% 3,3′-diaminobenzidine (DAB) and 0.003% H2O2 in 0.05 M Tris–HCl bufer (pH 7.5) for 5–10 min. Te sections were dehydrated in a graded series of ethanol, cleared with xylene and covered with DPX. Negative con- trol were performed by incubating sections without the primary antibodies. Immunohistochemical staining was evaluated by LeitzDialux 20 Microscope and photos were photographed by canon digital camera (Canon Power- shot A95) in the department of anatomy and histology, faculty of veterinary medicine, Assiut University, Egypt. Morphometric and statistical analysis. Te morphometric studies were performed on both light and immunohistochemical images of the camel cerebellum using Image-J sofware. Te dimensions and counting of the cells were performed by measuring at least 10 sections from every cerebellum, and the results were presented as the mean of the measurements and considered as representative at these regions. Te cross sectional area (CSA) is the measured area of the cells containing the whole view of the nucleus. Te diameters are the longest and shortest diameter of the cells, containing the complete view of the nucleus, passing through the nucleus. Te cellular density per CSA was performed by counting cells in a defned area and were fnally calculated to 0.01 mm2. Te linear density for PC was performed by counting the PC in a defned length of 1 mm.
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